Factors Contributing to Complete Oral Intake in Dysphagic Stroke Patients with Enteral Feeding Tubes in Convalescent Rehabilitation Wards

ABSTRACT

Objectives: This study investigated the factors contributing to complete oral intake (COI) in dysphagic stroke patients with enteral feeding tubes in the local clinical setting.

Methods: Data of patients with percutaneous endoscopic gastrostomy (PEG) or nasogastric tube (NGT) feeding on admission to convalescent rehabilitation wards (CRWs) were extracted from the Kaga Regional Cooperation Clinical Pathway for Stroke database for multiple centers including 19 acute care hospitals and 11 hospitals with CRWs. Patients were divided into two groups based on their status regarding COI or incomplete oral intake (ICOI) at discharge. Logistic regression analysis with forced-entry variables was used to identify factors contributing to COI.

Results: On discharge from CRWs, COI and ICOI were observed in 140 and 207 cases, respectively. The COI group was younger, had a higher rate of initial stroke, higher Functional Oral Intake Scale (FOIS) scores, higher Functional Independence Measure (FIM) motor and cognitive scores, higher Body Mass Index (BMI), lower rate of patients with PEG, and shorter stays in acute care wards. Logistic regression analysis with forced entry revealed that younger age; initial stroke; higher FOIS score, FIM cognitive score, and BMI; and shorter stay in the acute care ward contributed to COI.

Conclusions: The primary factors contributing to COI in dysphagic stroke patients with enteral feeding tubes were younger age, initial stroke, higher swallowing and cognitive function, good nutritional status, and shorter stay in the acute care ward.

INTRODUCTION

Dysphagia is one of the major complications after stroke, affecting 27%–64% of stroke patients.^1,2,3) Patients with inadequate oral nutrition may experience malnutrition, aspiration pneumonia, longer hospital stays, and a higher rate of mortality than their counterparts.^4,5,6) To avoid these complications, stroke patients with severe dysphagia need to be introduced to enteral tube feeding nutrition in the early stage after stroke onset.^7,8)

The main options for enteral feeding nutrition are percutaneous endoscopic gastrostomy (PEG) and nasogastric tube (NGT) feeding.^8,9) Because early initiation of PEG has been reported to increase the mortality rate and half of the patients with dysphagia will recover oral resumption, stroke patients with dysphagia who are unable to take enough nutrition orally are recommended to undergo NGT placement initially.^4,9,10) Conversely, previous studies have reported that continuous use of NGT feeding causes complications, such as nasal decubitus, reflux esophagitis, self-removal of the NGT, and aspiration pneumonia.^11,12,13,14) To avoid these complications, dysphagic stroke patients who do not regain their swallow function and require long-term enteral feeding are recommended to undergo PEG.^15,16) Therefore, physicians in acute care wards need to predict which dysphagic stroke patients will regain complete oral intake (COI) by recognizing the factors contributing to COI and appropriately assessing the indications for PEG.

Regarding the factors contributing to COI in stroke patients with enteral feeding tubes, some studies have shown that the severity of stroke and dysphagia contributed to incomplete oral intake (ICOI) at discharge from the acute care ward.^17,18,19,20) However, some patients classified as having persistent ICOI in acute care wards may recover to COI in convalescent rehabilitation wards (CRWs).²¹⁾ Several studies showed that the absence of aspiration, younger age, good nutrition status, and cognitive function contributed to achievement of COI at the time of discharge after the convalescent rehabilitation phase.^{22,23,24,25,26)} However, these previous studies were based on data obtained from a single center over a short period, and the results might not be applicable to dysphagic stroke patients in local clinical settings. Overall, these numerous preceding studies did not assess patients at the time of discharge from the CRW. As a result, the conclusions might not be applicable to stroke patients with enteral feeding tubes in the large population.

Therefore, in this study, we used the large database of the Kaga Regional Cooperation Clinical Pathway for Stroke (KRCCPS) featuring data collected over a prolonged period from multiple centers,^27,28,29,30) including 19 acute care hospitals and 11 hospitals with CRWs. The aim of this study was to investigate factors contributing to COI at the time of discharge from CRWs for stroke patients with enteral feeding tubes in the local clinical setting.

MATERIALS AND METHODS

Ethical Considerations

Written informed consent for using data from the KRCCPS database for stroke-related research was obtained from the patients and/or their legal guardians. All data derived from the KRCCPS database were anonymized, and the patient personal information was not identified. This study was approved by the Ethics Committee of Yawata Medical Center in Komatsu, Japan (Review No. 2022-01).

Study Design

In this case–control study, we divided patients into two groups based on whether they had regained COI or had ICOI at the time of discharge from the CRW. All patients were dependent on enteral feeding via PEG or an NGT at the time of admission to the CRW. For patients that were unable to take enough nutrition orally for more than 3 weeks, the physician in charge of the acute care ward recommended PEG to the patient and/or their key persons according to the guideline proposed by ESPEN.¹⁵⁾ The reasons for continuous use of NGT were: 1) rejection of PEG by patients and/or their legal guardians; 2) unknown willingness of patients and/or their legal guardians for PEG placement; 3) PEG placement being anatomically impossible; 4) unstable medical conditions for PEG; or 5) prospects for acquiring COI as judged by acute care physicians. We excluded: 1) patients transferred to acute care wards from CRWs or those who died in a CRW; 2) patients diagnosed with an epidural or subdural hematoma, because these types of strokes are likely to have different courses of recovery from cerebral infarction, cerebral hemorrhage, or subarachnoid hemorrhage³¹⁾; 3) stroke patients dependent on enteral feeding owing to comorbidities, such as neuromuscular diseases and upper digestive tract cancers; and 4) patients dependent on enteral feeding before stroke onset.

Database

Data collected over 10 years between January 2011 and December 2020 from KRCCPS were analyzed. The KRCCPS database was implemented in 2009 in the southern part of Ishikawa Prefecture in Japan, an area populated by about 1 million people. It contains data from 19 acute care hospitals, 11 hospitals with CRWs, and 466 facilities for community-based rehabilitation. This database contains patients’ characteristics and a wide range of stroke and rehabilitation-related evaluations from multiple medical staff members in acute care wards and CRWs. Details of the KRCCPS database have been described previously.^27,28,29,30)

All patients in the COI and ICOI groups received indirect and/or direct swallowing training from speech–language–hearing therapists in the CRWs. No patient had undergone balloon dilatation therapy, intermittent oro-esophageal tube feeding, or electrical stimulation therapy. All patients received therapy from physical and occupational therapists in the CRWs. The total training time from speech–language–hearing therapists, physical therapists, and occupational therapists for each patient was up to 180 min per day. All patients in the COI and ICOI groups underwent these sessions daily during CRW admission. The resumption of oral intake was decided by multidisciplinary teams in the CRWs based on the evaluation of the water swallowing test,³²⁾ food test,³³⁾ videofluorography, and/or video endoscopy results. The amount of nutrition and water was calculated using the Harris–Benedict formula,³⁴⁾ and body weight was monitored throughout hospitalization in both groups.

Variables and Measures

Age, sex, initial or recurrent stroke, and type of stroke (infarction, hemorrhage, or subarachnoid hemorrhage) were compared between the COI and ICOI groups. Some previous studies showed that patients with cerebral cortex injury, bilateral brain injury, and left-side brain injury have negative effects on the resumption of oral intake.^20,22,35) Therefore, we compared the incidences of cerebral cortex injury, bilateral injury, or the side of brain injury between the COI and ICOI groups. Because patients with infratentorial brain damage are reported to develop dysphagia,³⁶⁾ we compared the rate of supratentorial or infratentorial lesions between the COI and ICOI groups. The National Institutes of Health Stroke Scale (NIHSS) score³⁷⁾ was used to compare the severity of stroke between the groups. The NIHSS score was evaluated by the stroke treatment team in the acute care ward on the day of stroke onset. We used the Functional Oral Intake Scale (FOIS), which has a 7-grade scale of oral intake, to evaluate swallowing function. Scores less than 3 points indicate an enteral-tube-dependent individual, whereas more than 4 points indicates an individual who has achieved total oral intake. Interclass reliability and validity of the FOIS has been established in previous studies.^20,38,39) We defined COI as more than 4 points on the FOIS. The score of the Functional Independence Measure (FIM) was used to evaluate the level of activities of daily living (ADLs) in both groups. The FIM is a reliable, validated, and well-established scale of ADLs, including 13 items for motor function and 5 items for cognitive function.^40,41) Given that previous studies showed that malnutrition causes dysphagia,^26,42,43,44) we used Body Mass Index (BMI; kg/m²) to evaluate the nutritional status of both groups.⁴⁵⁾ The length of stay in the acute care ward was compared between the groups because CRWs can provide more intensive rehabilitation programs than acute care hospitals in Japan.²¹⁾ In addition, initiation of early rehabilitation were reported to contribute to better functional outcomes in patients with stroke.⁴⁶⁾ FOIS and FIM scores and BMI were evaluated by trained multidisciplinary teams in the CRWs.

Data Analysis

All quantitative data are expressed as median with interquartile range and were compared using the Mann–Whitney U-test. Categorical data are presented as numbers and were compared using the chi-square test. Variables with statistically significant differences between COI and ICOI were selected as independent factors that contributed to COI, and we performed logistic regression analysis with forced-entry variables. The variance inflation factor of each independent factor was calculated to avoid multicollinearity issues. We used SPSS version 26.0 for Windows (IBM, Armonk, NY, USA) to perform statistical analysis. Values of P<0.05 were considered significant.

RESULTS

We investigated 5502 patients from the KRCCPS database and found that 380 patients were dependent on enteral tube feeding at the time of admission to CRWs. There were 27 cases of missing data; 5 patients were transferred to acute care hospitals from CRWs, and 1 patient died in a CRW. Overall, we excluded 33 cases, and the remaining 347 cases were eligible for this study. At the time of discharge from the CRWs, COI was observed in 140 cases and ICOI was observed in 207 cases (Fig. 1).

Fig. 1.

Flowchart of patient selection criteria for the analysis.

The COI group had a lower age and lower rate of recurrent stroke than the ICOI group. There was no significant difference in sex, type of stroke (infarction, hemorrhage, or subarachnoid hemorrhage), lesion location, and NIHSS between the groups at the time of stroke onset (Table 1). Upon discharge from the acute care ward, the COI group had higher FOIS scores, higher FIM motor and cognitive scores, higher BMIs, and lower rates of PEG (26.13% vs 50%) than the ICOI group. In addition, the length of stay in the acute care ward for the COI group was 10 days shorter than that for the ICOI group (Table 2). At the time of discharge from the CRWs, the COI group had higher FOIS and FIM scores and a higher FIM score gain. BMIs were higher in the COI group, although BMI gain was lower than that in the ICOI group. No significant difference in the duration of CRW stay was observed between the COI and ICOI groups (Table 3).

Table 1. Characteristics of patients at onset of stroke

Characteristic	COI group (n=140)	ICOI group (n=207)	P value
Age (years)	74 (65–82)	79 (72–85)	<0.01**
Sex, male/female	65/75	105/102	0.45
Stroke incidence, initial/recurrent	113/27	139/68	<0.01**
Type of stroke, Infarction/hemorrhage/subarachnoid hemorrhage	47/74/19	96/85/26	0.052
Lesion location
Cerebral cortex injury, yes/no	64/76	107/100	0.33
Side of brain injury, right/left/both	52/66/22	76/82/49	0.16
Region, supratentorial/infratentorial	119/22	172/35	0.77
NIHSS score	20 (16–21)	20 (17–22)	0.46

Data is presented as median (interquartile range) or number.

Statistical significance: *P<0.05; **P<0.01.

Table 2. Characteristics of patients at time of admission to CRWs

Characteristic	COI group (n=140)	ICOI group (n=207)	P value
FOIS score	2 (1–2)	1 (1–2)	<0.01**
FIM motor score	13 (13–16)	13 (13–13)	<0.01**
FIM cognitive score	11 (6–15)	6 (5–10)	<0.01**
BMI (kg/m2)	21.5 (19.7–23.4)	20.0 (18.0–21.7)	<0.01**
Difference in enteral feeding tubes, PEG/NGT	29/111	69/138	<0.05*
Acute care ward stay (days)	34 (21–49)	44 (28–55)	<0.01**

Data is presented as median (interquartile range) or number.

Statistical significance: *P<0.05; **P<0.01.

Table 3. Characteristics of patients at time of discharge from CRWs

Characteristic	COI group (n=140)	ICOI group (n=207)	P value
FOIS score	6 (5–6)	1 (1–2)	<0.01**
FIM motor score	37 (22–59)	13 (13–16)	<0.01**
FIM motor score gain	21 (6–39)	0 (0–3)	<0.01**
FIM cognitive score	18 (12–26)	8 (5–12)	<0.01**
FIM cognitive score gain	5 (2–10)	1 (0–3)	<0.01**
BMI (kg/m2)	20.0 (18.4–22.0)	19.0 (17.5–20.7)	<0.01**
BMI gain	−1.2 (−2.6 to 0.3)	−0.7 (−1.8 to 0.0)	<0.01**
CRW stay (days)	143 (105–175)	133 (85–165)	0.07

Data is presented as median (interquartile range) or number.

Statistical significance: **P<0.01.

We selected age, initial or recurrent stroke, FOIS score, FIM motor and cognitive scores, BMI, difference in enteral feeding tubes (PEG or NGT), and length of acute care ward stay as independent factors contributing to COI at the day of discharge. Because the variance inflation factors for all independent factors were less than 1.7, we considered all of them to be acceptable candidates for independent factors influencing outcomes. Logistic regression analysis with forced entry revealed that younger age, initial stroke, high FOIS and FIM cognitive scores, higher BMI, and shorter stay in acute care wards contributed to COI on the day of discharge from the CRWs. The difference in enteral feeding method (PEG or NGT) did not contribute to COI (Table 4).

Table 4. Results of logistic regression analysis with forced entry

Characteristic	β	Odds ratio	95% CI	P value
Age (years)	–0.05	0.96	[0.93–0.98]	<0.01**
Stroke incidence, initial/recurrent	1.12	3.05	[1.59–5.84]	<0.01**
FOIS score	1.18	3.25	[2.04–5.16]	<0.01**
FIM motor score	0.04	1.04	[0.98–1.10]	0.16
FIM cognitive score	0.10	1.11	[1.04–1.17]	<0.01**
BMI (kg/m2)	0.15	1.16	[1.06–1.28]	<0.01**
Difference in enteral feeding tubes, PEG/NGT	0.43	1.54	[0.82–2.88]	0.16
Acute care ward stay (days)	−0.03	0.97	[0.96–0.99]	<0.01**

CI, confidence interval.

**Statistical significance: **P<0.01.

DISCUSSION

In this study, we showed that younger age, initial stroke, higher FOIS score, higher cognitive FIM score, higher BMI, and shorter stay in the acute care ward all contributed to recommencement of COI on discharge from the CRW. These results are concordant with those of previous large studies.^{26,35,42,43,44,46,47,48,49,50,51)}

It has been reported that younger patients have more neuroplasticity and are more likely to regain swallowing function than elderly patients,^44,47,49) and patients with initial stroke have more residual neurological function, are less likely to have pseudobulbar palsy, and are more likely to regain swallowing function than those with recurrent stroke.³⁵⁾ Patients with preserved swallowing and cognitive functions achieve COI more easily during swallowing training than those without, and such preservation increases the likelihood of reacquisition of COI.^{26,44,47,48,49)} We could not assess higher brain dysfunction because almost all of the patients in this study had severe strokes. However, higher brain function in cases with severe stroke could be evaluated through observation such as cognitive FIM scores for identifying factors contributing to COI.⁵²⁾ Previous studies have found a relationship among malnutrition, BMI, and dysphagia as well as between sarcopenia and dysphagia.^{26,42,43,44,50)} Some patients in this study might have had sarcopenia, although we could not diagnose patients with sarcopenia because almost all patients in our study had severe disabilities that prevented the evaluation of gait speed or grip power. Evaluation of sarcopenia before stroke onset might be needed to identify whether sarcopenia affects COI in stroke patients with enteral feeding tubes. A review reported that early initiation of swallowing training leads to higher improvement in patient swallowing function.^46,51) In the current study, patients who had shorter stays in acute care wards had early initiation of swallowing training in the CRWs, which might have led to a higher chance of COI.

Type of stroke and lesion location did not contribute to COI in a statistically significant manner, although the number of patients with cerebral hemorrhage was higher in the COI group. Numerous previous studies have reported conflicting results about the relationship among the type of stroke, lesion location and dysphagia.^{20,22,35,36,53,54,55,56)} Crisan et al. showed that recovery of swallowing was more frequent for hemorrhagic stroke patients than for those suffering ischemic stroke.⁵³⁾ However, Jørgensen et al. and Andersen et al. reported more severe outcomes associated with hemorrhagic strokes than with ischemic strokes.^54,55) Moon et al. reported that swallowing disturbance is related to infratentorial brain lesions.³⁶⁾ However, Pombo et al. observed no significant relationship between brain lesion location and swallowing function.⁵⁶⁾ All these previous studies were based on small sample sizes, including patients with variable swallowing functions and infarct volumes. Prospective studies with large sample sizes that can accurately assess lesion location and size are needed to identify the correlations among the type of stroke, location and size of brain injury, and recovery of oral COI in dysphagic stroke patients with enteral feeding tubes.

No previous study has found enteral feeding method (PEG or NGT) to be an independent factor contributing to COI. Wang et al. and Nam et al. showed that NGT placement in the throat causes laryngeal edema that can lead to blocking of laryngeal elevation and cause swallowing difficulties.^57,58) However, they based their conclusions on patient swallowing function evaluated using video fluorography and/or video endoscopy before and after NGT removal; they did not investigate whether continuous NGT placement impeded COI at the time of discharge. Several other studies reported that there was no principal obstacle to starting oral feeding in stroke patients with properly placed NGTs.^59,60,61) In our study, 249 dysphagic stroke patients with NGT placement received swallowing training from speech–language–hearing therapists, and 111 patients (44.58%) achieved COI at discharge from the CRW. Regarding PEG, 29 of 98 patients (29.59%) achieved COI, which was a lower response than that in patients with NGT. In addition, the variable of the difference in enteral feeding tubes (PEG or NGT) at the time of admission to CRWs did not contribute to COI according to the logistic regression analysis with forced entry. It is clear that the placement of an NGT in the patient larynx did not hamper swallowing training and did not impede COI achievement at the time of discharge from the CRW.

Our current study identified that younger age, initial stroke, higher FOIS score, higher FIM cognitive score, higher BMI, and shorter stay in the acute care ward contributed to the resumption of COI. Consequently, physicians in acute care wards may be able to predict whether dysphagic stroke patients with enteral feeding tubes will be able to resume COI by considering their age, swallowing function, cognitive function, and nutritional status when determining whether PEG is indicated. If patients are predicted to achieve COI, they do not have to undergo PEG. However, if patients are predicted to continue ICOI, they should undergo PEG to avoid aspiration pneumonia and self-removal of the NGT in the CRW.²⁷⁾ The formula for the prediction of achieving COI has been reported in previous studies.^20,26,44,62)

Our study has several limitations, mainly because of its retrospective design. First, the type of enteral feeding tube (PEG or NGT) was not allocated randomly. However, PEG indication was based on the guidelines proposed by ESPEN,¹⁵⁾ and the rejection of PEG by the patient and/or their legal guardian led to continuous use of NGT. We adjusted patient stroke severity by logistic regression analysis with forced entry and found that the difference in enteral feeding tube (PEG or NGT) did not contribute to COI. Therefore, the non-randomized study design might not have affected our results. Second, we could not ascertain whether the NGT was placed properly in the throat so that it did not interfere with swallowing training, and the differences of NGTs in CRWs might affect the outcomes. However, given that patients with NGTs achieved COI more frequently than those with PEG, we deemed that these patients received appropriate NGT insertion and management in the CRWs. Third, there were variations in swallowing training and nursing care among the CRWs in this study, which might have affected patients’ recovery of COI. Nevertheless, the CRWs in our study were certified by the Japanese Ministry of Health and Labor and provided standard rehabilitation training and care; therefore, it is unlikely that the difference in CRWs affected our conclusion. Fourth, we did not investigate the impacts of comorbidities and pharmaceuticals on COI. In a previous study, Lee et al. investigated whether comorbidities, such as hypertension, atrial fibrillation, diabetes mellitus, alcohol, and smoking affected COI, but reported that younger age and good functional status contributed to COI.²⁵⁾ It has been reported that angiotensin-converting enzyme inhibitors and cilostazol can prevent aspiration pneumonia.^63,64) However, to the best of our knowledge, no study has identified specific medications that affected the resumption of COI. Consequently, it is unlikely that comorbidities or medication affected our results.

CONCLUSION

This study is the first to identify factors contributing to COI in stroke patients with enteral feeding tubes at the time of discharge from CRWs in local clinical settings. Our results provide evidence to physicians determining the appropriate enteral feeding method (PEG or NGT) for patients with dysphagic stroke who were unable to tolerate sufficient oral nutrition.

CONFLICTS OF INTEREST

The authors declare no conflicts of interest.

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